Genetic diversity and relationships of the liver fluke Fasciola hepatica (Trematoda) with native and introduced definitive and intermediate hosts

Fasciolosis is a worldwide spread parasitosis mainly caused by the trematode Fasciola hepatica. This disease is particularly important for public health in tropical regions, but it can also affect the economies of many developed countries due to large infections in domestic animals. Although several studies have tried to understand the transmission by studying the prevalence of different host species, only a few have used population genetic approaches to understand the links between domestic and wildlife infections. Here, we present the results of such genetic approach combined with classical parasitological data (prevalence and intensity) by studying domestic and wild definitive hosts from Camargue (southern France) where fasciolosis is considered as a problem. We found 60% of domestic hosts (cattle) infected with F. hepatica but lower values in wild hosts (nutria, 19%; wild boars, 4.5%). We explored nine variable microsatellite loci for 1,148 adult flukes recovered from four different populations (non-treated cattle, treated cattle, nutria and wild boars). Populations from the four groups differed, though we found a number of migrants particularly non-treated cattle and nutria. Overall, we detected 729 different multilocus genotypes (from 783 completely genotyped individuals) and only 46 genotypes repeated across samples. Finally, we experimentally infected native and introduced intermediate snail hosts to explore their compatibility with F. hepatica and assess the risks of fasciolosis expansion in the region. The introduced species Galba truncatula and Pseudosuccinea columella attained the higher values of overall compatibility in relation to the European species. However, concerning the origin, sympatric combinations of G. truncatula were more compatible (higher prevalence, intensity and survival) than the allopatric tested. According to our results, we should note that the assessment of epidemiological risks cannot be limited to a single host–parasite system, but should focus on understanding the diversity of hosts in the heterogeneous environment through space and time.Fil: Vázquez, Antonio A.. Instituto de Medicina Tropical “Pedro Kourí”; Cuba. Université Montpellier II; Francia. Centre National de la Recherche Scientifique; FranciaFil: Sabourin, Emeline. Centre National de la Recherche Scientifique; Francia. Université Montpellier II; FranciaFil: Alda, Maria del Pilar. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Bahía Blanca; Argentina. Universidad Nacional del Sur. Departamento de Biología, Bioquímica y Farmacia. Laboratorio de Zoología de Invertebrados I; Argentina. Centre National de la Recherche Scientifique; Francia. Université Montpellier II; FranciaFil: Leroy, Clémentine. Centre National de la Recherche Scientifique; Francia. Université Montpellier II; FranciaFil: Leray, Carole. Institut de Recherche de la Tour du Valat; FranciaFil: Carron, Eric. Centre National de la Recherche Scientifique; Francia. Université Montpellier II; FranciaFil: Mulero, Stephen. Centre National de la Recherche Scientifique; Francia. Université Montpellier II; Francia. Université de Perpignan Via Domitia; FranciaFil: Caty, Céline. Institut de Recherche de la Tour du Valat; FranciaFil: Hasfia, Sarah. Centre National de la Recherche Scientifique; Francia. Université Montpellier II; FranciaFil: Boisseau, Michel. Centre National de la Recherche Scientifique; Francia. Université Montpellier II; FranciaFil: Saugné, Lucas. Centre National de la Recherche Scientifique; Francia. Université Montpellier II; FranciaFil: Pineau, Olivier. Institut de Recherche de la Tour du Valat; FranciaFil: Blanchon, Thomas. Institut de Recherche de la Tour du Valat; FranciaFil: Alba, Annia. Instituto de Medicina Tropical “Pedro Kourí”; Cuba. Università di Corsica Pasquale Paoli; FranciaFil: Faugère, Dominique. Centre National de la Recherche Scientifique; Francia. Université Montpellier II; FranciaFil: Vittecoq, Marion. Centre National de la Recherche Scientifique; Francia. Université Montpellier II; Francia. Institut de Recherche de la Tour du Valat; FranciaFil: Hurtrez Boussès, Sylvie. Centre National de la Recherche Scientifique; Francia. Université Montpellier II; Franci

Fasciola hepatica's dynamic in intensive anthropized system : la Camargue

L’émergence et la ré-émergence de maladies que nous connaissons depuis ces cents dernières années représentent une véritable crise sanitaire en grande partie due aux perturbations anthropiques qui modifient les écosystèmes et les interactions entre les parasites et leurs hôtes. La prévention et le contrôle des maladies infectieuses nécessitent la compréhension de leur dynamique dans l’ensemble des compartiments dans lesquels elles circulent. Parmi ces maladies, la fasciolose est une maladie particulièrement sensible aux changements liés à l’Homme. Cette zoonose causée par le parasite Fasciola hepatica, est communément reconnue comme un problème vétérinaire, mais aussi de santé publique, dans certaines régions du monde. Notre étude vise à comprendre la dynamique de circulation et les risques d'émergence de la fasciolose dans un contexte de forte anthropisation. Il s'agit (1) d'étudier la dynamique de l’hôte intermédiaire, un mollusque de la famille des lymnaieidae. (2) de comprendre la dynamique et la diversité du parasite entre et au sein de ses différents compartiments hôtes définitifs. Ces travaux ont été menés sur le territoire camarguais sur le domaine de la Tour du Valat, nous permettant d’avoir accès aux hôtes définitifs, sauvages (ragondins et sangliers), domestiques (taureaux traités et non traités) et à l’hôte intermédiaire, Galba truncatula appelé communément limnée tronquée. Dans un premier temps, nous avons caractérisé la végétation des habitats favorables à la présence du mollusque et nous avons trouvé que les mares semblaient être des zones présentant un risque plus important que les canaux d’irrigation pour la transmission de la fasciolose. Puis, nous nous sommes intéressée à l’influence des habitats sur la dynamique de G. truncatula par des approches de génétique des populations. Nos résultats ont permis de montrer que la permanence des habitats et la connectivité influencent le mode de reproduction, la structuration des populations et la dispersion des limnées en Camargue. Dans un second temps, nous avons étudié la dynamique et la circulation du parasite au sein du compartiment hôte définitif. Nos résultats de la génétique des populations du parasite chez les hôtes définitifs, nous ont indiqué qu’il existait sur notre site d’étude plusieurs sites de transmission constituant un seul grand foyer global. Par ailleurs, l’étude de la circulation du parasite entre les hôtes définitifs suggère le rôle des sangliers dans la dispersion de la maladie et le rôle des ragondins dans le maintien du cycle de la fasciolose. Cette étude met en évidence l’intérêt de mener des études à long terme et l’importance de prendre en compte tous les compartiments impliqués pour comprendre l’épidémiologie d’une maladie. Elle souligne également le rôle des activités humaines et de l’écosystème dans la dynamique de la fasciolose. Le but final de cette étude est de proposer une gestion intégrée adaptée au contexte camarguais afin de limiter l’impact sanitaire de la fasciolose mais aussi des autres maladies liées à l’élevage dans cette région.The emergence and re-emergence of diseases encountered over the last hundred years represent a real health crisis largely due to anthropic disturbances that affect the ecosystems as well as the interactions between parasites and hosts. The prevention and control of emerging infectious diseases require an in-depth understanding of their dynamics in all the compartments in which they occur. Among these diseases, Fasciolosis is particularly sensitive to human related changes. This zoonosis caused by the parasite Fasciola hepatica, is commonly recognized as a veterinary problem and major public health issue in certain countries. Our study aims to understand the circulation dynamics and risks of fasciolosis emergence in a context of high anthropization. Our objective is (1) to study the dynamics of the intermediate host, a mollusc of the lymnaieidae family. (2) to understand the dynamics and diversity of the parasite between and within its different definitive host compartments. This work was carried out in the Camargue in the Tour du Valat estate, allowing us to have access to the definitive hosts, wild (nutria and wild boars), domestic (treated and untreated bulls) and the intermediate host, Galba truncatula. First, we characterized the habitats that are favorable to the intermediate host G. truncatula, presence in Camargue and we found that ponds appear to be areas of higher risk than irrigation channels for fasciolosis transmission. Then, we became interested in the influence of habitats on the dynamics of G. truncatula through population genetics approaches, our results showed that habitat permanence and connectivity influence the reproduction mode, population structure and dispersal of G. truncatula in the Camargue. In a second step, we studied the dynamics and circulation of the parasite within the definitive host compartment. Our results of the population genetic analyses of definitive hosts indicated that there were several transmission sites on our study area that constituted a single large global outbreak. In addition, the study of the circulation of the parasite between wildlife and domestic animals suggests the role of wild boars in the spread of the disease and the role of nutrias in maintaining the fasciolosis cycle. Our work highlights the value of long term studies and the importance of taking into account all the compartments involved to understand the epidemiology of a disease. They also emphasize the role of human activities and ecosystem in the dynamics of fasciolosis. The ultimate goal of this study is to propose integrated management measures adapted to the Camargue context in order to limit the health impact of fasciolosis and other livestock diseases in the region

Dynamique de la fasciolose dans un système fortement anthropisé : la Camargue

The emergence and re-emergence of diseases encountered over the last hundred years represent a real health crisis largely due to anthropic disturbances that affect the ecosystems as well as the interactions between parasites and hosts. The prevention and control of emerging infectious diseases require an in-depth understanding of their dynamics in all the compartments in which they occur. Among these diseases, Fasciolosis is particularly sensitive to human related changes. This zoonosis caused by the parasite Fasciola hepatica, is commonly recognized as a veterinary problem and major public health issue in certain countries. Our study aims to understand the circulation dynamics and risks of fasciolosis emergence in a context of high anthropization. Our objective is (1) to study the dynamics of the intermediate host, a mollusc of the lymnaieidae family. (2) to understand the dynamics and diversity of the parasite between and within its different definitive host compartments. This work was carried out in the Camargue in the Tour du Valat estate, allowing us to have access to the definitive hosts, wild (nutria and wild boars), domestic (treated and untreated bulls) and the intermediate host, Galba truncatula. First, we characterized the habitats that are favorable to the intermediate host G. truncatula, presence in Camargue and we found that ponds appear to be areas of higher risk than irrigation channels for fasciolosis transmission. Then, we became interested in the influence of habitats on the dynamics of G. truncatula through population genetics approaches, our results showed that habitat permanence and connectivity influence the reproduction mode, population structure and dispersal of G. truncatula in the Camargue. In a second step, we studied the dynamics and circulation of the parasite within the definitive host compartment. Our results of the population genetic analyses of definitive hosts indicated that there were several transmission sites on our study area that constituted a single large global outbreak. In addition, the study of the circulation of the parasite between wildlife and domestic animals suggests the role of wild boars in the spread of the disease and the role of nutrias in maintaining the fasciolosis cycle. Our work highlights the value of long term studies and the importance of taking into account all the compartments involved to understand the epidemiology of a disease. They also emphasize the role of human activities and ecosystem in the dynamics of fasciolosis. The ultimate goal of this study is to propose integrated management measures adapted to the Camargue context in order to limit the health impact of fasciolosis and other livestock diseases in the region.L’émergence et la ré-émergence de maladies que nous connaissons depuis ces cents dernières années représentent une véritable crise sanitaire en grande partie due aux perturbations anthropiques qui modifient les écosystèmes et les interactions entre les parasites et leurs hôtes. La prévention et le contrôle des maladies infectieuses nécessitent la compréhension de leur dynamique dans l’ensemble des compartiments dans lesquels elles circulent. Parmi ces maladies, la fasciolose est une maladie particulièrement sensible aux changements liés à l’Homme. Cette zoonose causée par le parasite Fasciola hepatica, est communément reconnue comme un problème vétérinaire, mais aussi de santé publique, dans certaines régions du monde. Notre étude vise à comprendre la dynamique de circulation et les risques d'émergence de la fasciolose dans un contexte de forte anthropisation. Il s'agit (1) d'étudier la dynamique de l’hôte intermédiaire, un mollusque de la famille des lymnaieidae. (2) de comprendre la dynamique et la diversité du parasite entre et au sein de ses différents compartiments hôtes définitifs. Ces travaux ont été menés sur le territoire camarguais sur le domaine de la Tour du Valat, nous permettant d’avoir accès aux hôtes définitifs, sauvages (ragondins et sangliers), domestiques (taureaux traités et non traités) et à l’hôte intermédiaire, Galba truncatula appelé communément limnée tronquée. Dans un premier temps, nous avons caractérisé la végétation des habitats favorables à la présence du mollusque et nous avons trouvé que les mares semblaient être des zones présentant un risque plus important que les canaux d’irrigation pour la transmission de la fasciolose. Puis, nous nous sommes intéressée à l’influence des habitats sur la dynamique de G. truncatula par des approches de génétique des populations. Nos résultats ont permis de montrer que la permanence des habitats et la connectivité influencent le mode de reproduction, la structuration des populations et la dispersion des limnées en Camargue. Dans un second temps, nous avons étudié la dynamique et la circulation du parasite au sein du compartiment hôte définitif. Nos résultats de la génétique des populations du parasite chez les hôtes définitifs, nous ont indiqué qu’il existait sur notre site d’étude plusieurs sites de transmission constituant un seul grand foyer global. Par ailleurs, l’étude de la circulation du parasite entre les hôtes définitifs suggère le rôle des sangliers dans la dispersion de la maladie et le rôle des ragondins dans le maintien du cycle de la fasciolose. Cette étude met en évidence l’intérêt de mener des études à long terme et l’importance de prendre en compte tous les compartiments impliqués pour comprendre l’épidémiologie d’une maladie. Elle souligne également le rôle des activités humaines et de l’écosystème dans la dynamique de la fasciolose. Le but final de cette étude est de proposer une gestion intégrée adaptée au contexte camarguais afin de limiter l’impact sanitaire de la fasciolose mais aussi des autres maladies liées à l’élevage dans cette région

Impact of Human Activities on Fasciolosis Transmission

International audienceFasciolosis is a worldwide disease caused by the liver fluke Fasciola spp. This food- and water-borne disease is a major public health and veterinary issue. It is currently (re)emerging in several regions mainly due to the rapid evolution of human activities. This article reviews the current knowledge of the impact of irrigation-system management, livestock management, and human diet and hygiene habits on the emergence of fasciolosis. We also identify the gaps in this knowledge and the possible solutions for limiting these impacts. Integrated control seems to be the most effective solution for controlling fasciolosis, because it enables monitoring, prevention, and rapid action in case of the (re)emergence of the disease

Lymnaeid snails hosts of Fasciola hepatica and Fasciola gigantica (Trematoda: Digenea): A worldwide review

Fasciolosis is a snail-borne disease, causing serious public and veterinary health problems worldwide. This disease is produced by infection with Fasciola hepatica or Fasciola gigantica through the consumption of vegetables or water contaminated with the parasite’s metacercarial cysts. Both species of liver flukes are transmitted worldwide by small freshwater snails of the family Lymnaeidae. A global account on the species that are actually or may act as potential hosts of Fasciola spp., compiling particular research on their geographical distribution and susceptibility, is needed as a helpful tool in the understanding of fasciolosis transmission, and therefore in the control and prevention programmes of the disease. We have gathered here a comprehensive review of those lymnaeid species that are known to transmit the parasites in the field or that have been experimentally tested. We aim to bring forward the main intermediate hosts by regions in order to facilitate the understanding of worldwide transmission.Fil: Vázquez, Antonio A.. University of Montpellier; Francia. Instituto de Medicina Tropical Pedro Kouri; CubaFil: Alda, Maria del Pilar. University of Montpellier; Francia. Universidad Nacional del Sur; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Lounnas, Manon. University of Montpellier; FranciaFil: Sabourin, Emeline. University of Montpellier; Francia. Institut de recherche de la Tour du Valat; FranciaFil: Alba, Annia. Instituto de Medicina Tropical Pedro Kouri; CubaFil: Pointier, Jean Pierre. Université de Perpignan; FranciaFil: Hurtrez-Boussès, Sylvie. University of Montpellier; Franci

Balanced Polymorphism at the Pgm-1 Locus of the Pompeii Worm Alvinella pompejana and Its Variant Adaptability Is Only Governed by Two QE Mutations at Linked Sites

International audienceThe polychaete Alvinella pompejana lives exclusively on the walls of deep-sea hydrothermal chimneys along the East Pacific Rise (EPR), and displays specific adaptations to withstand the high temperatures and hypoxia associated with this highly variable habitat. Previous studies have revealed the existence of a balanced polymorphism on the enzyme phosphoglucomutase associated with thermal variations, where allozymes 90 and 100 exhibit different optimal activities and thermostabilities. Exploration of the mutational landscape of phosphoglucomutase 1 revealed the maintenance of four highly divergent allelic lineages encoding the three most frequent electromorphs over the geographic range of A. pompejana. This polymorphism is only governed by two linked amino acid replacements, located in exon 3 (E155Q and E190Q). A two-niche model of selection, including ‘cold’ and ‘hot’ conditions, represents the most likely scenario for the long-term persistence of these isoforms. Using directed mutagenesis and the expression of the three recombinant variants allowed us to test the additive effect of these two mutations on the biochemical properties of this enzyme. Our results are coherent with those previously obtained from native proteins, and reveal a thermodynamic trade-off between protein thermostability and catalysis, which is likely to have maintained these functional phenotypes prior to the geographic separation of populations across the Equator about 1.2 million years ago

Fasciola hepatica-Pseudosuccinea columella interaction: effect of increasing parasite doses, successive exposures and geographical origin on the infection outcome of susceptible and naturally-resistant snails from Cuba

Abstract Background Pseudosuccinea columella is one of the most widespread vectors of Fasciola hepatica, a globally distributed trematode that affects humans, livestock and wildlife. The exclusive occurrence in Cuba of susceptible and naturally-resistant populations to F. hepatica within this snail species, offers a fascinating model for evolutionary biology, health sciences and vector control strategies. In particular, resistance in P. columella is characterized by the encapsulation of the parasite by host’s immune cells and has been experimentally tested using different Cuban F. hepatica isolates with no records of successful infection. Here, we aimed to explore for the first time, the effect of different parasite doses, successive exposures and different parasite origins on the infection outcomes of the two phenotypes of P. columella occurring in Cuba. Methods To increase the chances for F. hepatica to establish, we challenged Cuban P. columella with increasing single parasite doses of 5, 15 or 30 miracidia and serial exposures (three-times) of 5 miracidia using a sympatric F. hepatica isolate from Cuba, previously characterized by microsatellite markers. Additionally, we exposed the snails to F. hepatica from different geographical origins (i.e. Dominican Republic and France). Parasite prevalence, redial burden and survival of snails were recorded at 25 days post-exposure. Results No parasite development was noted in snails from the resistant populations independent of the experimental approach. Contrastingly, an overall increase in prevalence and redial burden was observed in susceptible snails when infected with high miracidia doses and after serial exposures. Significant differences in redial burden between single 15 miracidia and serial 3 × 5 miracidia infected snails suggest that immune priming potentially occurs in susceptible P. columella. Compatibility differences of allopatric (Caribbean vs European) F. hepatica with susceptible snails were related to the geographical scale of the combinations. Conclusions Here, the effectiveness of P. columella resistance to F. hepatica does not decline with increasing parasite doses, successive infection or different geographical origins of parasite isolates, while presenting new evidence for specificity for infection in susceptible P. columella snails. Understanding the peculiarities of the P. columella-F. hepatica interaction and the extent of the resistant phenotype is crucial for an effective parasite control and for developing alternatives to tackle fasciolosis transmission

Reviewing Fasciola hepatica transmission in the West Indies and novel perceptions from experimental infections of sympatric vs. allopatric snail/fluke combinations

International audienceFasciolosis is an important food-borne parasitic disease affecting over two million people worldwide with economic losses related to cattle production of up to US$ 3 billion annually. Despite the long known presence of Fasciola hepatica in the Caribbean islands its transmission is not well known. This study reviews historical and recent data on fasciolosis in the West Indies, revealing for the first time the outcomes of sympatric and allopatric fluke/snail interactions in the area by exploring the susceptibility of four lymnaeid species after exposure to F. hepatica isolates from Cuba, the Dominican Republic and France. Overall, Galba cubensis showed a mean prevalence of 71.8% and appears to be the most suitable intermediate host species irrespective of the isolate used. Sympatric combinations (snail and parasite from the same country) were generally more compatible (higher susceptibility, parasite intensity and snail survival post-exposure) and only the allopatric interaction of French G. truncatula/Cuban F. hepatica attained 100% prevalence and mean intensity over 33 rediae/snail. However, certain Dominican populations of Pseudosuccinea columella showed high parasite intensities (>30 rediae/snail) when infected with Cuban flukes, highlighting the potential risks of biological introductions. Overall, high compatibility in most sympatric combinations compared to low or moderate compatibility in allopatric ones, suggests the existence of local adaptation from a long sustained interaction that has led to high rates of transmission. Interestingly, attempts to infect G. schirazensis with sympatric and allopatric flukes failed and coupled with the lowest survival rates which supposes a low risk of fasciolosis transmission in areas where this is the only snail species. Although there are significant gaps in the actual status of fasciolosis transmission from several islands in the West Indies these results show a permanent risk. We conclude that fasciolosis transmission is high in areas where the local snail, G. cubensis, occurs, and will be even higher in the presence of the invasive P. columella